Quantitative principles of cis-translational control by general mRNA sequence features in eukaryotes
Abstract
General translational cis-elements are present in the mRNAs of all genes and affect the recruitment, assembly, and progress of preinitiation complexes and the ribosome under many physiological states. These elements include mRNA folding, upstream open reading frames, specific nucleotides flanking the initiating AUG codon, protein coding sequence length, and codon usage. The quantitative contributions of these sequence features and how and why they coordinate to control translation rates are not well understood.
- Authors:
-
[3]
- University of California, Los Angeles, CA (United States). Department of Statistics, Department of Biomathematics, and Department of Human Genetics
- Fred Hutchinson Cancer Research Center, Seattle, WA (United States). Computational Biology Program, Public Health Sciences and Basic Sciences Division
- Lawrence Berkeley National Laboratory, Berkeley, CA (United States). Biological Systems and Engineering Division
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1626948
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genome Biology (Online)
- Additional Journal Information:
- Journal Name: Genome Biology (Online); Journal Volume: 20; Journal Issue: 1; Journal ID: ISSN 1474-760X
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- Biotechnology & Applied Microbiology; Genetics & Heredity
Citation Formats
Li, Jingyi Jessica, Chew, Guo-Liang, and Biggin, Mark Douglas. Quantitative principles of cis-translational control by general mRNA sequence features in eukaryotes. United States: N. p., 2019.
Web. doi:10.1186/s13059-019-1761-9.
Li, Jingyi Jessica, Chew, Guo-Liang, & Biggin, Mark Douglas. Quantitative principles of cis-translational control by general mRNA sequence features in eukaryotes. United States. https://doi.org/10.1186/s13059-019-1761-9
Li, Jingyi Jessica, Chew, Guo-Liang, and Biggin, Mark Douglas. Fri .
"Quantitative principles of cis-translational control by general mRNA sequence features in eukaryotes". United States. https://doi.org/10.1186/s13059-019-1761-9. https://www.osti.gov/servlets/purl/1626948.
@article{osti_1626948,
title = {Quantitative principles of cis-translational control by general mRNA sequence features in eukaryotes},
author = {Li, Jingyi Jessica and Chew, Guo-Liang and Biggin, Mark Douglas},
abstractNote = {General translational cis-elements are present in the mRNAs of all genes and affect the recruitment, assembly, and progress of preinitiation complexes and the ribosome under many physiological states. These elements include mRNA folding, upstream open reading frames, specific nucleotides flanking the initiating AUG codon, protein coding sequence length, and codon usage. The quantitative contributions of these sequence features and how and why they coordinate to control translation rates are not well understood.},
doi = {10.1186/s13059-019-1761-9},
journal = {Genome Biology (Online)},
number = 1,
volume = 20,
place = {United States},
year = {2019},
month = {8}
}
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Works referenced in this record:
TRANSLATIONAL REGULATION OF GCN4 AND THE GENERAL AMINO ACID CONTROL OF YEAST
journal, October 2005
- Hinnebusch, Alan G.
- Annual Review of Microbiology, Vol. 59, Issue 1
Determinants of translation efficiency and accuracy
journal, January 2011
- Gingold, Hila; Pilpel, Yitzhak
- Molecular Systems Biology, Vol. 7, Issue 1
Control of Translation and miRNA-Dependent Repression by a Novel Poly(A) Binding Protein, hnRNP-Q
journal, May 2013
- Svitkin, Yuri V.; Yanagiya, Akiko; Karetnikov, Alexey E.
- PLoS Biology, Vol. 11, Issue 5
Poly(A)-tail profiling reveals an embryonic switch in translational control
journal, January 2014
- Subtelny, Alexander O.; Eichhorn, Stephen W.; Chen, Grace R.
- Nature, Vol. 508, Issue 7494
Multiple roles of the coding sequence 5′ end in gene expression regulation
journal, December 2014
- Tuller, Tamir; Zur, Hadas
- Nucleic Acids Research, Vol. 43, Issue 1
Connections Underlying Translation and mRNA Stability
journal, September 2016
- Radhakrishnan, Aditya; Green, Rachel
- Journal of Molecular Biology, Vol. 428, Issue 18
Translational control by 5'-untranslated regions of eukaryotic mRNAs
journal, June 2016
- Hinnebusch, A. G.; Ivanov, I. P.; Sonenberg, N.
- Science, Vol. 352, Issue 6292
mRNA length-sensing in eukaryotic translation: reconsidering the “closed loop” and its implications for translational control
journal, December 2016
- Thompson, Mary K.; Gilbert, Wendy V.
- Current Genetics, Vol. 63, Issue 4
Gene length as a regulator for ribosome recruitment and protein synthesis: theoretical insights
journal, December 2017
- Fernandes, Lucas D.; Moura, Alessandro P. S. de; Ciandrini, Luca
- Scientific Reports, Vol. 7, Issue 1
Quantitating translational control: mRNA abundance-dependent and independent contributions and the mRNA sequences that specify them
journal, October 2017
- Li, Jingyi Jessica; Chew, Guo-Liang; Biggin, Mark D.
- Nucleic Acids Research, Vol. 45, Issue 20
Translation efficiency is a determinant of the magnitude of miRNA-mediated repression
journal, November 2017
- Cottrell, Kyle A.; Szczesny, Pawel; Djuranovic, Sergej
- Scientific Reports, Vol. 7, Issue 1
Rate-Limiting Steps in Yeast Protein Translation
journal, June 2013
- Shah, Premal; Ding, Yang; Niemczyk, Malwina
- Cell, Vol. 153, Issue 7
Improved Ribosome-Footprint and mRNA Measurements Provide Insights into Dynamics and Regulation of Yeast Translation
journal, February 2016
- Weinberg, David E.; Shah, Premal; Eichhorn, Stephen W.
- Cell Reports, Vol. 14, Issue 7
Ribosome profiling reveals the rhythmic liver translatome and circadian clock regulation by upstream open reading frames
journal, October 2015
- Janich, Peggy; Arpat, Alaaddin Bulak; Castelo-Szekely, Violeta
- Genome Research, Vol. 25, Issue 12
mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
journal, July 2016
- Eichhorn, Stephen W.; Subtelny, Alexander O.; Kronja, Iva
- eLife, Vol. 5
Conservation of uORF repressiveness and sequence features in mouse, human and zebrafish
journal, May 2016
- Chew, Guo-Liang; Pauli, Andrea; Schier, Alexander F.
- Nature Communications, Vol. 7, Issue 1
Deciphering the rules by which 5'-UTR sequences affect protein expression in yeast
journal, July 2013
- Dvir, S.; Velten, L.; Sharon, E.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 30
Quantitative analysis of mammalian translation initiation sites by FACS ‐seq
journal, August 2014
- Noderer, William L.; Flockhart, Ross J.; Bhaduri, Aparna
- Molecular Systems Biology, Vol. 10, Issue 8
Rationally designed, heterologous S. cerevisiae transcripts expose novel expression determinants
journal, July 2015
- Ben-Yehezkel, Tuval; Atar, Shimshi; Zur, Hadas
- RNA Biology, Vol. 12, Issue 9
Deep learning of the regulatory grammar of yeast 5′ untranslated regions from 500,000 random sequences
journal, November 2017
- Cuperus, Josh T.; Groves, Benjamin; Kuchina, Anna
- Genome Research, Vol. 27, Issue 12
Alternative transcription start site selection leads to large differences in translation activity in yeast
journal, October 2012
- Rojas-Duran, M. F.; Gilbert, W. V.
- RNA, Vol. 18, Issue 12
Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources
journal, April 2014
- Li, Gene-Wei; Burkhardt, David; Gross, Carol
- Cell, Vol. 157, Issue 3
Mammalian microRNAs predominantly act to decrease target mRNA levels
journal, August 2010
- Guo, Huili; Ingolia, Nicholas T.; Weissman, Jonathan S.
- Nature, Vol. 466, Issue 7308
Translational Landscape of Photomorphogenic Arabidopsis
journal, October 2013
- Liu, Ming-Jung; Wu, Szu-Hsien; Wu, Jing-Fen
- The Plant Cell, Vol. 25, Issue 10
Effects of cycloheximide on the interpretation of ribosome profiling experiments in Schizosaccharomyces pombe
journal, September 2017
- Duncan, Caia D. S.; Mata, Juan
- Scientific Reports, Vol. 7, Issue 1
Super-resolution ribosome profiling reveals unannotated translation events in Arabidopsis
journal, October 2016
- Hsu, Polly Yingshan; Calviello, Lorenzo; Wu, Hsin-Yen Larry
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 45
Translational contributions to tissue specificity in rhythmic and constitutive gene expression
journal, June 2017
- Castelo-Szekely, Violeta; Arpat, Alaaddin Bulak; Janich, Peggy
- Genome Biology, Vol. 18, Issue 1
Stability of ribonucleic acid double-stranded helices
journal, July 1974
- Borer, Philip N.; Dengler, Barbara; Tinoco, Ignacio
- Journal of Molecular Biology, Vol. 86, Issue 4
Characterization of RNA hairpin loop stability
journal, January 1988
- Groebe, Duncan R.; Uhlenbeck, Olke C.
- Nucleic Acids Research, Vol. 16, Issue 24
Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure
journal, May 1999
- Mathews, David H.; Sabina, Jeffrey; Zuker, Michael
- Journal of Molecular Biology, Vol. 288, Issue 5
ViennaRNA Package 2.0
journal, November 2011
- Lorenz, Ronny; Bernhart, Stephan H.; Höner zu Siederdissen, Christian
- Algorithms for Molecular Biology, Vol. 6, Issue 1
Thermodynamic Parameters for an Expanded Nearest-Neighbor Model for Formation of RNA Duplexes with Watson−Crick Base Pairs †
journal, October 1998
- Xia, Tianbing; SantaLucia, John; Burkard, Mark E.
- Biochemistry, Vol. 37, Issue 42
An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs
journal, January 1987
- Kozak, Marilyn
- Nucleic Acids Research, Vol. 15, Issue 20
A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation
journal, September 2014
- Gingold, Hila; Tehler, Disa; Christoffersen, Nanna R.
- Cell, Vol. 158, Issue 6
An Evolutionarily Conserved Mechanism for Controlling the Efficiency of Protein Translation
journal, April 2010
- Tuller, Tamir; Carmi, Asaf; Vestsigian, Kalin
- Cell, Vol. 141, Issue 2
Speeding with control: codon usage, tRNAs, and ribosomes
journal, November 2012
- Novoa, Eva Maria; Ribas de Pouplana, Lluís
- Trends in Genetics, Vol. 28, Issue 11
Widespread Translational Remodeling during Human Neuronal Differentiation
journal, November 2017
- Blair, John D.; Hockemeyer, Dirk; Doudna, Jennifer A.
- Cell Reports, Vol. 21, Issue 7
Tunable protein synthesis by transcript isoforms in human cells
journal, January 2016
- Floor, Stephen N.; Doudna, Jennifer A.
- eLife, Vol. 5
Transcriptome analysis of human tissues and cell lines reveals one dominant transcript per gene
journal, January 2013
- Gonzàlez-Porta, Mar; Frankish, Adam; Rung, Johan
- Genome Biology, Vol. 14, Issue 7
Alternative start and termination sites of transcription drive most transcript isoform differences across human tissues
journal, November 2017
- Reyes, Alejandro; Huber, Wolfgang
- Nucleic Acids Research, Vol. 46, Issue 2
A high quality Arabidopsis transcriptome for accurate transcript-level analysis of alternative splicing
journal, April 2017
- Zhang, Runxuan; Calixto, Cristiane P. G.; Marquez, Yamile
- Nucleic Acids Research, Vol. 45, Issue 9
Impact of regulatory variation from RNA to protein
journal, December 2014
- Battle, Alexis; Khan, Zia; Wang, Sidney H.
- Science, Vol. 347, Issue 6222
Codon Optimality Is a Major Determinant of mRNA Stability
journal, March 2015
- Presnyak, Vladimir; Alhusaini, Najwa; Chen, Ying-Hsin
- Cell, Vol. 160, Issue 6
miRBase: annotating high confidence microRNAs using deep sequencing data
journal, November 2013
- Kozomara, Ana; Griffiths-Jones, Sam
- Nucleic Acids Research, Vol. 42, Issue D1
MicroRNAs AND THEIR REGULATORY ROLES IN PLANTS
journal, June 2006
- Jones-Rhoades, Matthew W.; Bartel, David P.; Bartel, Bonnie
- Annual Review of Plant Biology, Vol. 57, Issue 1
A compendium of RNA-binding motifs for decoding gene regulation
journal, July 2013
- Ray, Debashish; Kazan, Hilal; Cook, Kate B.
- Nature, Vol. 499, Issue 7457
Eukaryotic start and stop translation sites
journal, January 1991
- Cavener, Douglas R.; Ray, Stuart C.
- Nucleic Acids Research, Vol. 19, Issue 12
Diversity of preferred nucleotide sequences around the translation initiation codon in eukaryote genomes
journal, November 2007
- Nakagawa, S.; Niimura, Y.; Gojobori, T.
- Nucleic Acids Research, Vol. 36, Issue 3
Specific functional interactions of nucleotides at key -3 and +4 positions flanking the initiation codon with components of the mammalian 48S translation initiation complex
journal, March 2006
- Pisarev, A. V.
- Genes & Development, Vol. 20, Issue 5
Stretching of Homopolymeric RNA Reveals Single-Stranded Helices and Base-Stacking
journal, April 2007
- Seol, Yeonee; Skinner, Gary M.; Visscher, Koen
- Physical Review Letters, Vol. 98, Issue 15
The control of flux
journal, May 1995
- Kacser, H.; Burns, J. A.; Kacser, H.
- Biochemical Society Transactions, Vol. 23, Issue 2
Ribosome Collision Is Critical for Quality Control during No-Go Decay
journal, October 2017
- Simms, Carrie L.; Yan, Liewei L.; Zaher, Hani S.
- Molecular Cell, Vol. 68, Issue 2
Translation drives mRNA quality control
journal, June 2012
- Shoemaker, Christopher J.; Green, Rachel
- Nature Structural & Molecular Biology, Vol. 19, Issue 6
On the Ribosomal Density that Maximizes Protein Translation Rate
journal, November 2016
- Zarai, Yoram; Margaliot, Michael; Tuller, Tamir
- PLOS ONE, Vol. 11, Issue 11
The ribosomal protein genes and Minute loci of Drosophila melanogaster
journal, January 2007
- Marygold, Steven J.; Roote, John; Reuter, Gunter
- Genome Biology, Vol. 8, Issue 10
An in vivo control map for the eukaryotic mRNA translation machinery
journal, January 2013
- Firczuk, Helena; Kannambath, Shichina; Pahle, Jürgen
- Molecular Systems Biology, Vol. 9, Issue 1
Diurnal Oscillations in Liver Mass and Cell Size Accompany Ribosome Assembly Cycles
journal, May 2017
- Sinturel, Flore; Gerber, Alan; Mauvoisin, Daniel
- Cell, Vol. 169, Issue 4
Quantitating Protein Synthesis, Degradation, and Endogenous Antigen Processing
journal, March 2003
- Princiotta, Michael F.; Finzi, Diana; Qian, Shu-Bing
- Immunity, Vol. 18, Issue 3
A quantitative estimation of the global translational activity in logarithmically growing yeast cells
journal, October 2008
- von der Haar, Tobias
- BMC Systems Biology, Vol. 2, Issue 1
System wide analyses have underestimated protein abundances and the importance of transcription in mammals
journal, January 2014
- Li, Jingyi Jessica; Bickel, Peter J.; Biggin, Mark D.
- PeerJ, Vol. 2
A Comprehensive tRNA Deletion Library Unravels the Genetic Architecture of the tRNA Pool
journal, January 2014
- Bloom-Ackermann, Zohar; Navon, Sivan; Gingold, Hila
- PLoS Genetics, Vol. 10, Issue 1
Accurate design of translational output by a neural network model of ribosome distribution
journal, July 2018
- Tunney, Robert; McGlincy, Nicholas J.; Graham, Monica E.
- Nature Structural & Molecular Biology, Vol. 25, Issue 7
Statistics requantitates the central dogma
journal, March 2015
- Li, J. J.; Biggin, M. D.
- Science, Vol. 347, Issue 6226
Estimating Translational Selection in Eukaryotic Genomes
journal, November 2008
- dos Reis, M.; Wernisch, L.
- Molecular Biology and Evolution, Vol. 26, Issue 2
The frailty of adaptive hypotheses for the origins of organismal complexity
journal, May 2007
- Lynch, M.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue Supplement 1
Mean of the Typical Decoding Rates: A New Translation Efficiency Index Based on the Analysis of Ribosome Profiling Data
journal, December 2014
- Dana, Alexandra; Tuller, Tamir
- G3: Genes|Genomes|Genetics, Vol. 5, Issue 1
Upstream ORF s are prevalent translational repressors in vertebrates
journal, February 2016
- Johnstone, Timothy G.; Bazzini, Ariel A.; Giraldez, Antonio J.
- The EMBO Journal, Vol. 35, Issue 7
codes_for_general_mRNA_sequence_features_in_five_eukaryotes
other, January 2019
- Li, Jingyi Jessica
- Zenodo
Short poly(A) tails are a conserved feature of highly expressed genes
journal, November 2017
- Lima, Sarah Azoubel; Chipman, Laura B.; Nicholson, Angela L.
- Nature Structural & Molecular Biology, Vol. 24, Issue 12
eIF4B stimulates translation of long mRNAs with structured 5′ UTRs and low closed-loop potential but weak dependence on eIF4G
journal, September 2016
- Sen, Neelam Dabas; Zhou, Fujun; Harris, Michael S.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 38
Human 5′ UTR design and variant effect prediction from a massively parallel translation assay
journal, July 2019
- Sample, Paul J.; Wang, Ban; Reid, David W.
- Nature Biotechnology, Vol. 37, Issue 7
AGO-bound mature miRNAs are oligouridylated by TUTs and subsequently degraded by DIS3L2
journal, June 2020
- Yang, Acong; Shao, Tie-Juan; Bofill-De Ros, Xavier
- Nature Communications, Vol. 11, Issue 1
System Wide Analyses have Underestimated Protein Abundances and the Importance of Transcription in Mammals
text, January 2012
- Li, Jingyi Jessica; Bickel, Peter J.; Biggin, Mark D.
- arXiv
Works referencing / citing this record:
Quantitative global studies reveal differential translational control by start codon context across the fungal kingdom
journal, February 2020
- Wallace, Edward W. J.; Maufrais, Corinne; Sales-Lee, Jade
- Nucleic Acids Research, Vol. 48, Issue 5
G-quadruplex located in the 5′UTR of the BAG-1 mRNA affects both its cap-dependent and cap-independent translation through global secondary structure maintenance
journal, September 2019
- Jodoin, Rachel; Carrier, Julie C.; Rivard, Nathalie
- Nucleic Acids Research, Vol. 47, Issue 19
Bacterial contribution to genesis of the novel germ line determinant oskar
journal, February 2020
- Blondel, Leo; Jones, Tamsin EM; Extavour, Cassandra G.
- eLife, Vol. 9